Miguel A. L. Nicolelis
Department of Neurobiology, Duke University Medical Center
The rat trigeminal somatosensory system was used a model to investigate how populations of neurons, located at multiple processing stages of the a sensory pathway, represent sensory information following passive and active tactile stimulation. Contrary to the traditional view of this sensory system, our results revealed the existence of highly dynamic and distributed representations of tactile information, not only in the somatosensory cortex, but also in the thalamus and even in the brainstem. In these structures, we identified broadly tuned neurons with multiwhisker receptive fields (RFs). In the thalamus, a large percentage of neurons exhibited shifts in the spatial domain of their RFs as a function of post-stimulus time. During these shifts, the center of the neuron's RF moved across the whisker pad from caudal to rostral whiskers, but not in the opposite direction, suggesting that these spatiotemporal RFs may encode directional information. Simultaneous recordings of the activity of cortical and thalamic neurons carried out by Asif Ghazanfar, a graduate student in our laboratory, revealed that thalamocortical ensemble responses increase in a nonlinear fashion according to the extent and spatial orientation of the multiple-whisker stimuli. Supralinear responses were seen more frequently with vertically- than horizontally-oriented stimuli suggesting that thalamocortical interactions generate complex spatial transformations and that these are used by rats for tactile discrimination.
Further investigation by Barbara Faggin, a postdoctoral fellow, revealed that cortical and subcortical somatosensory representations are maintained by dynamic interactions between multiple convergent afferents, since they could be altered in a matter of seconds by reversible peripheral sensory deprivations. The dynamic organization of thalamic and cortical maps seems to be shaped since early postnatal life by tactile experience. This conclusion was derived from experiments carried out by Laura Oliveira, a postodoctoral fellow, and Marshal Shuller, a graduate student. In these experiments, complete unilateral sections of the facial nerve were produced on PND 10. This manipulation, which eliminated the ipsilateral production of rhythmic whisker movements used by rats to actively explore objects, leads to significant functional modifications in the contralateral VPM thalamus and SI cortex. These included a reduction in thalamic and cortical receptive fields, elimination of thalamic RF shifts, reduction in thalamocortical ensemble response summation to multiwhisher stimuli, and narrowing of the frequency tuning curves of cortical neurons.
In collaboration with John Chapin and Rick Lin, we also investigated the dynamic properties of the rat trigeminal system in behaving animals. During active tactile exploration, we observed that cortical, thalamic, and brainstem neurons can exhibit widespread 7-12 Hertz synchronous oscillations, which began during attentive immobility and reliably predicted the imminent onset of rhythmic whisker twitching. Initially, each oscillatory cycle began as a traveling wave of neural activity in cortex and then spread to the thalamus. Just prior to onset of rhythmic whisking, the oscillations spread to the spinal trigeminal brainstem complex. Thereafter, the oscillations at all levels were synchronous with whisker protraction. We interpreted these results as evidence that distributed synchronous activity in the trigeminal system may encode not only sensory information but also the onset and temporal domain of tactile exploratory movements. Further experiments carried out by Erika Fanselow and Merri Rose, two graduate students, revealed that sensory responses throughout the thalamocortical loop may vary significantly during the presence of these oscillations. Overall, these results suggest that the rat somatosensory system relies on both spatial and temporal interactions between populations of cortical and subcortical neurons to process tactile information during natural exploratory behaviors.